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Hetero-specific queen retinue behavior of worker bees in
mixed-species colonies of Apis cerana and Apis mellifera
Ming-Xian Yang, Ken Tan, Sarah E. Radloff, Christian W.W. Pirk, H.
Randall Hepburn
To cite this version:
Original article
Hetero-specific queen retinue behavior of worker bees
in mixed-species colonies of Apis cerana and Apis mellifera
*
Ming-Xian Y
ang
1,2, Ken T
an
2, Sarah E. R
adloff
3, Christian W.W. P
irk
4,
H. Randall H
epburn
1,21Department of Zoology and Entomology, Rhodes University, Grahamstown 6140, Republic of South Africa 2Eastern Bee Research Institute, Yunnan Agricultural University, Heilongtan, Kunming, Yunnan Province,
P.R. China
3Department of Statistics, Rhodes University, Grahamstown 6140, Republic of South Africa 4Department of Zoology and Entomology, Social Insect Research Group, University of Pretoria 0002 Pretoria,
Republic of South Africa
Received 18 March 2009 – Revised 5 May 2009 – Accepted 6 May 2009
Abstract – The retinue behavior of worker bees of Apis cerana cerana and Apis mellifera ligustica in
two types of mixed-species colonies were studied to determine whether observed behaviors are pre- or post-speciation developments. In A. cerana queen-led mixed colonies, almost equal numbers of A. cerana workers (53.4±7.4) and A. mellifera workers (51.2±8.1) attended the A. cerana queen; while in A. mellifera queen-led mixed colonies, the A. mellifera queen attracted significantly fewer (47.8±5.9) A. cerana workers than A. mellifera workers (51.9±4.6). Thus about 100 workers in total were attracted to each queen. In pure
A. cerana and A. mellifera colonies, the queen attracted 105.8 ± 9.1 and 107.8 ± 11.2 workers, respectively,
there being no significant difference between them. Only the pheromones 9-ODA, 9-HDA and 10-HDA of the queens were significantly different and the workers did not show avoidance behavior to either hetero-specific queen. Both species of workers were attracted by the queens and engaged in retinue behavior, suggesting that the retinue response was not related to a specific queen pheromone or colony environment. This non-specific queen retinue behavior in the mixed colonies indicates that the queen pheromones can be transmitted among the workers from the two species without any obstacles. We conclude that retinue be-havior itself as well as the pheromones of the queens that induce this bebe-havior are both primitive, conserved traits that preceded speciation in apine bees.
Apis cerana/ Apis mellifera / retinue behavior / queen pheromones
1. INTRODUCTION
Retinue behavior is fundamental and cru-cial to the biology of socru-cial insects because queens must be attended to ensure functional-ity of colonies. “Retinue” behavior [= “court behavior”, Allen, 1955, 1960; = “attending behavior”, Sakagami, 1958; Velthuis, 1972] refers to the behavior of worker honeybees, Corresponding author: Sarah Radloff,
s.radloff@ru.ac.za; Ken Tan, eastbee@public.km.yn.cn
* Manuscript editor: Stan Schneider
Apis spp., that form a loose circle facing in
toward their queen. These bees feed and fre-quently lick her, but soon leave the circle to be replaced by others (Ribbands,1953; Allen,
1955). As the queen moves over the comb, most of the workers who encounter her show a distinct interest, and extend their antennae and palpate her (Butler, 1954; Sakagami, 1958). Naumann et al. (1991) demonstrated that these retinue bees obtain pheromones from the body of the queen and pass them trophallactically to other workers. Although the wax combs in honeybee colonies also play a role in queen pheromone transfer (Hepburn, 1998),
Honeybee retinue behavior 55
the retinue bees are the principal transmitters (Naumann et al.,1991). Consequently, as the first group of receivers and messengers, the retinue bees play a key role in pheromonally transmitting the queen’s presence throughout the colony (Seeley, 1979; Naumann et al.,
1991; Pankiw et al.,1995).
The pheromones of a queen which at-tract workers and induce retinue behav-ior include secretions from the mandibular glands and Dufour’s gland (Slessor et al.,
1988; Kaminski et al., 1990; Pankiw et al.,
1995; Katzav-Gozansky et al., 2003). In ret-inue bioassays with A. cerana workers, only three constituents of the mandibular gland pheromones were sufficient to elicit full ret-inue behavior (Plettner et al., 1997). Al-though A. cerana, is a sister-species of A.
mellifera, having diverged only about 3
mil-lion years ago (Arias and Sheppard, 1996,
2005), some behavioral traits and morpho-logical characteristics of the two species are very similar indeed, and, clearly are highly conserved, pre-speciation traits. Among them are pheromones of their respective queens, which share most, but not all, chemical con-stituents of the mandibular glad pheromonal bouquet (Plettner et al., 1997). For example methyl oleate, coniferyl alcohol, and linolenic acid appear unique to A. mellifera (Keeling et al.,2003). However, reciprocal assays to as-sess whether retinue behavior can be induced within a heterospecific context, such that A.
cerana queens attract A. mellifera workers and A. mellifera queens A. cerana workers remain
to be performed.
Mixed-species colonies offer an intriguing model to investigate the behavioral relation-ships of the two species, and to suggest which features are ancestral to the common ancestor of A. cerana and A. mellifera and which may have preceded speciation. As examples, while there are dialectical differences in the waggle dances of different species (Lindauer, 1957; Dyer and Seeley,1991; Dyer,2002), it has re-cently been demonstrated independently that heterospecific dance communication is oper-ative in both A. cerana and A. mellifera (Su et al., 2008; Tan et al., 2008). Returning to pheromones, it remains to be seen whether heterospecific retinue behavior is shared in
A. cerana and A. mellifera, and if so, would
such behavior aid in the dispersal of the queen pheromones, or would the ‘guest’ species in such mixed colonies avoid the host queen in order to escape pheromonal control (Moritz et al., 2001; Neumann and Moritz,2002). A plausible theoretical background for possible differences in heterospecific retinues would lead to the hypothesis that we would expect no differences in the proportions of A.
cer-ana and A. mellifera workers attending
het-erospecific queens versus conspecific queens. In which case, a complete lack of differences would indicate that retinue behavior had devel-oped prior to speciation; and small differences would indicate very recent changes in the sys-tem. The results could indicate whether any aspects of retinue behavior are pre- or post-speciation developments.
2. MATERIALS AND METHODS 2.1. Honeybee colonies
The experiments and observations were con-ducted with colonies of Apis cerana cerana and
Apis mellifera ligustica at an apiary of Yunnan
Agricultural University, Kunming, China. In order to avoid differing amounts of queen pheromones owing to possible age effects, all queens tested were between 300-330 days old (Pankiw et al., 1995) and all queens had headed their colonies for 10 months.
2.2. Organization of the mixed colonies
Two types of mixed colonies were established: mixed colonies containing worker brood of both A.
cerana and A. mellifera and were headed by A. cer-ana queens; and mixed colonies containing worker
these colonies. The colonies were checked daily and the time when the empty combs had been filled with newly laid eggs was recorded so we knew when the developing bees would eclose as young adults. These combs were kept in the parental colonies un-til they developed into capped pupae and were then transferred into incubators.
Then the, three A. mellifera and three A.
cer-ana, colonies were chosen as host colonies for
es-tablishing mixed-species colonies. These colonies were small, about 1500 individuals, mostly young adults (the older field bees having been eliminated by relocating the hives). These host colonies also had equal numbers of their own sealed pupae about to emerge, so a cohort of workers of the same age of both species could be obtained at the same time. Three days before the young adults would emerge, these brood frames were introduced into hetero-specific host colonies i.e. one A. mellifera comb was put into each of the three A. cerana colonies and one A. cerana combs into each of the A.
mel-lifera colonies. Newly emerged young adult bees
are readily accepted by the host colonies and so the mixed colonies are constituted (Tan et al.,2006). Three pure A. mellifera colonies and three A.
cer-ana colonies served as control groups and each
con-tained enough newly emerging adult workers of the same age as those which were introduced into inter-specific colonies.
Although the mixed colonies were constituted by an unequal number of host (adult+ emerging) and introduced (only emerging) workers, this ought not to have an effect on retinue composition be-cause queen attendance by workers is strongly age-dependent, with 3–9 days being the age range for intense contact with the queen (Seeley,1979).
2.3. Monitoring the retinue behavior in the mixed-species colonies
Once the mixed colonies were settled, the intro-duced workers were adults about a fortnight old. In our observations, only those workers that attended a queen for at least 5 seconds were regarded as ret-inue bees (modified from Pankiw et al.,1995) be-cause the queens were allowed to roam freely on the frames. Queen retinue behavior of the workers was recorded with a video camera for five minutes in each of the mixed and control colonies once a day for seven days. Therefore, it was possible to very ac-curately count the numbers of bees of each species in a particular retinue at any given time. Using a
5 sec contact paradigm for retinue bee recognition and a viewing window of 5 min over 7 days, the retinue data set was just about 420 observations per colony. We took the videos between 1400 h–1700 h in the afternoon.
The queens were allowed to roam freely on the comb during which one group of retinue bees were left behind and new ones formed a new retinue circle. The colonies were kept in normal standard hives so that we were able to take videos only by opening the hive and taking out the combs care-fully, but no matter how gentle we were, all the queens stopped egg-laying and were seen roaming in our video clips. So, the five minutes cumulative numbers are obviously greater than what one might see at any instant. Therefore numbers were derived from worker turnover around the queen. We did not mark the bees individually in the hive because we could not know which bees would join a retinue, but we were able to eliminate pseudo-replication counts by replaying the video clips in a lower speed.
2.4. Pheromone analysis
Honeybee retinue behavior 57
A.cerana worker A.mellifera worker A.cerana queen
Figure 1. A. cerana queen attended by A. mellifera
and A. cerana worker bees in an A. cerana queen-led mixed colony.
2.5. Data analysis
Independent samples T-tests were used to com-pare the mean number and proportions of the ret-inue workers to different queens. Homogeneity of the variances between groups was checked using Levene’s test. Differences in the proportions of each component of queen pheromones were tested using independent T-tests, and a multivariate ANOVA test was used to test for overall differences in mandibu-lar gland components between A. cerana and A.
mellifera queens. The means and standard
devia-tions of each variable were calculated. All tests were performed using Statisticac (StatSoft,2008).
3. RESULTS
3.1. Queen retinue behavior between colonies
In A. cerana queen-led mixed colonies, al-most equal proportions of A. cerana workers (0.51 ± 0.04) and A. mellifera workers (0.49 ± 0.04) attended the A. cerana queens (Fig. 1) and the results were not significantly different (t = 1.32, df = 20, P = 0.202, Tab.I). In A.
mellifera queen-led mixed colonies a
signifi-cantly smaller proportion of A. cerana work-ers, (0.48 ± 0.04), than A. mellifera workwork-ers, (0.52 ± 0.04), attended the A. mellifera queen (Fig.2) (t= 2.71, df = 20, P = 0.014, Tab.I).
Comparing the number of retinue bees to different types of queens, in A. cerana queen-led mixed colonies, 53.4±7.4 A. cerana work-ers were attracted by the A. cerana queen, whilst A. mellifera queens in A. mellifera
A.mellifera worker A.cerana worker
A.mellifera queen
Figure 2. A. mellifera queen attended by A.
cer-ana and A. mellifera worker bees in an A. mellifera
queen-led mixed colony.
queen-led mixed colonies attracted signifi-cantly fewer A. cerana worker bees (47.8 ± 5.9, t = 2.74, df = 40, P = 0.009). As for the
A. mellifera worker bees, 51.2 ± 8.1 attended A. cerana queens and 51.9 ± 4.6 attended A. mellifera queens, there was no significant
dif-ference (t= 0.33, df = 40, P = 0.744). When the total numbers of workers (A.
cer-ana + A. mellifera) attracted to a retinue of A. cerana queens were compared with those
attracted to A. mellifera queens, in A.
cer-ana queen-led mixed colonies, an average of
104.6 ± 13.3 workers were observed in ret-inues around the A. cerana queen, while in
A. mellifera queen-led mixed colonies, the A. mellifera queen attracted 99.7 ± 7.8 retinue
bees. The values are not significantly differ-ent. (t = 1.49, df = 40, P = 0.145). In pure
A. cerana and A. mellifera colonies, the queen
attracted 105.8 ± 9.1 and 107.8 ± 11.2 work-ers, respectively, there being no significant dif-ference between them (t = 0.62, df = 40,
P= 0.538).
There was a significant difference between the mean number of workers that A.
mellif-era queens attracted, 99.7 ± 7.8, in A. mellif-era queen-led mixed colonies and A. mellifmellif-era
queen attracted in pure colonies, 107.8 ± 11.2 (t = 2.74, df = 40, P = 0.009). There was no significant difference between the mean num-ber of workers that A. cerana queens attracted, 104.6 ± 13.3 in A. cerana queen-led mixed colonies and A. cerana queen attracted in pure colonies, 105.8 ± 9.1, (t = 0.34, df = 40,
Table I. Mean number and proportion of retinue bees (± SD) attracted to the queens for each group.
A. cerana queen-led A. mellifera queen-led Pure A. Pure A.
mixed colonies mixed colonies cerana mellifera
colonies colonies
A. cerana A. mellifera A. cerana A. mellifera A. cerana A. mellifera
Col. retinue retinue retinue retinue retinue retinue
1 56.4 ± 6.4 54.9 ± 6.4 49.4 ± 6.6 50.4 ± 3.1 101.9 ± 4.9 103.9 ± 7.6 2 46.6 ± 4.6 42.9 ± 4.7 44.4 ± 5.7 51.0 ± 5.0 109.1 ± 10.0 107.3 ± 12.5 3 57.3 ± 6.0 55.9 ± 5.9 49.4 ± 4.6 54.1 ± 5.1 106.4 ± 11.0 112.1 ± 12.6
x± SD 53.4 ± 7.4 51.2 ± 8.1 47.8 ± 5.9 51.9 ± 4.6 105.8 ± 9.1 107.8 ± 11.2
Proportion 0.51 ± 0.04 0.49 ± 0.04 0.48 ± 0.04 0.52 ± 0.04 workers showed no ovarian activity or
egg-laying under the host queens.
3.2. Pheromones
The proportional values of the pheromonal components of the queens in the two types of mixed colonies were analyzed, and the re-sults are shown in TableII. The results of mul-tivariate ANOVA procedures to test for dif-ferences in proportional values of mandibular gland components between A. mellifera and
A. cerana showed a significant overall di
ffer-ence (Wilk’s lambda: F = 741.6, df = 4, 1,
P = 0.027, Tab. II). Two of these compo-nents, HOB and 10-HDAA did not differ be-tween species; however, 9-ODA, 9-HDA and 10-HDA differed significantly (9-ODA: t = 6.5, df = 4, P = 0.003; 9-HDA: t = 7.4, df= 4, P = 0.002; 10-HDA: t = 3.5, df = 4,
P = 0.024). The ratio of pheromonal
compo-nents 9-ODA/(9-ODA+10-HDA+10-HDAA) was significantly higher in A. cerana queens than in A. mellifera queens (t = 3.0, df = 4,
P= 0.041, Tab.II).
4. DISCUSSION 4.1. Queen pheromones
Our results show that the proportional val-ues of three of the pheromonal components from A. mellifera and A. cerana queens (9-ODA, 9-HDA and 10-HDA) differed signifi-cantly (Tab. II). The proportional values for
A. mellifera queens obtained here are within
the range of those reported in the literature (Crewe and Velthuis, 1980; Slessor et al.,
1988; Naumann et al., 1991; Pankiw et al.,
1995; Hoover,2005). Quantitative analysis of the amounts showed that A. cerana queens have significantly less of the QMS components than A. mellifera (Tab.II). This result is con-sistent with previous investigations (Plettner et al.,1997; Free,1987). These results confirm that there are high levels of variation between individuals, and possibly between different races. Possible environmental effects in the production of queens’ pheromones are ruled out because comparisons of the heterospecific queen pheromones do not differ from those of normal queens for each species.
We argue that the basic queen signal-ing mechanism is conserved and queen pheromones and retinue formation preceded speciation in Apis because workers of both species respond to heterospecific queens. However, there is a pheromonal nuance be-cause A. cerana workers responded less to
A. mellifera queens and there are
Honeybee retinue behavior 59
Table II. Mean± SD weight (µg) and proportional values of mandibular gland components of mixed
colonies A. cerana and A. mellifera queens (N= 3, each).
Component A. cerana A. mellifera P∗
weight (µg) proportion weight (µg) proportion 4-methyl-hydroxy-benzoate 49.98 ± 17.48 0.16 ± 0.06 38.71 ± 7.05 0.08 ± 0.01 0.103 (HOB) 9 -keto-2(E)-decenoic acid 232.07 ± 27.55 0.71 ± 0.04 244.13 ± 30.27 0.52 ± 0.03 0.002 (9-ODA) 9-hydroxy-2(E)-decenoic acid 31.92 ± 10.80 0.10 ± 0.03 147.47 ± 21.54 0.31 ± 0.04 0.002 (9-HDA) 10-hydroxydecanoic acid 6.17 ± 3.51 0.02 ± 0.01 13.71 ± 9.50 0.03 ± 0.02 0.512 (10-HDAA) 10-hydroxy-2(E)-decenoic 4.26 ± 0.99 0.01 ± 0.00 25.91 ± 10.29 0.06 ± 0.02 0.024 acid (10-HDA)
Multivariate test of all 0.027†
components
Ratio:9-ODA/9-ODA+ 0.96 ± 0.02 0.86 ± 0.05 0.041
10-HDA+10-HDAA
* Probability from univariate t−tests (df = 4). † Wilk’s lambda (df = 4,1).
in the two species while the queens of one of these species produce more pheromone? and (2) why do A. mellifera queens attract fewer workers in mixed colonies compared to pure colonies?
4.2. Queen retinue behavior
Workers form a retinue around the queen in all honeybee species thus far examined (Verheijen-Voogd,1959; Free,1987; Plettner et al., 1997). But, bioassay-guided identifi-cation of retinue-active compounds has only been done in A. mellifera (Kaminski et al.,
1990; Plettner et al., 1997; Keeling et al.,
2003). So, the exact compounds responsible for retinue behavior in A. cerana are unknown (Plettner et al., 1997, Keeling et al., 2001). Under experimental conditions, Plettner et al. (1997) found that the retinue response of A.
cerana workers to QMP blends with and
with-out HVA did not differ significantly, suggest-ing that HVA is not required for maximal worker attraction in A. cerana. However, this result can not exclude the possibility that this component is not necessary for A. mellifera workers to be attracted to exhibit retinue be-havior. Because cuticular hydrocarbons also
play a role in the recognition systems of in-sects (Singer,1998), and especially so in hon-eybees (Breed,1998) this possibility must be addressed. We discount any importance of cu-ticular hydrocarbons in retinue behavior in this case because queens being superseded do not attract retinues because of a pheromonal insuf-ficiency (Slessor et al.,1988) while pheromon-ally queen-like workers (pseudoqueens) do (Moritz et al.,2000).
In our study, we tested the responses of workers of both species to hetero-specific queens, and found that three pheromonal com-ponents of the queens were significantly differ-ent, 9-ODA, 9-HDA and 10-HDA (cf. Tab.II). The other compounds of the QMP are very similar, and the workers did not show any obvious avoidance behavior to either of the hetero-specific queens. Both species were at-tracted by the queens, engaged in retinue be-havior, licked the queens and showed normal grooming and feeding behavior. These results suggest that the retinue response was not re-lated to a specific queen pheromone or colony environment, and this is consistent with the results of other investigations (Pankiw et al.,
transmitted among the workers from the two species without any obstacles, irrespective of possible “suppressive agents” (Fletcher and Ross,1985) or “honest signals” (Peeters et al.,
1999; Strauss et al., 2008). Workers showed no ovarian activity or egg-laying under the host queens (Tan et al., unpubl. data). We con-clude that retinue behavior itself as well as the pheromones of the queens that induce this be-havior are both ancestral, conserved traits that preceded speciation in apine bees.
ACKNOWLEDGEMENTS
Financial support was granted to Mingxian Yang by the Yunnan Agricultural University of China.
Comportement de cour des ouvrières d’abeilles envers la reine de l’autre espèce dans des colonies mixtes d’Apis cerana et Apis mellifera.
Apis cerana/ Apis mellifera / comportement de
cour/ ouvrière / phéromone de la reine
Zusammenfassung – Hofstaatverhalten von Ar-beiterinnen in gemischten Apis cerana/Apis
mellifera-Völkern. Mittels reziproker
Versuchsan-sätze untersuchten wir, ob Hofstaatverhalten in ei-nem heterospezifischen Kontext ausgelöst werden kann, d.h., ob Apis cerana Königinnen attraktiv sein können für Apis mellifera Arbeiterinnen und umgekehrt, ob dies auch bei A. mellifera Königin-nen und A. cerana ArbeiterinKönigin-nen der Fall ist. Diese Versuche führten wir in zwei Mischvölkern beste-hend aus A. cerana und A. mellifera Arbeiterinnen durch. In Mischvölkern mit einer A. cerana Köni-gin fanden wir etwa gleiche Proportionen von A.
cerana (53,4 ± 7,4) und A. mellifera Arbeiterinnen
(51,2 ± 8,1) im Hofstaat. In Mischvölkern mit einer
A. mellifera Königin hingegen waren dort
signifi-kant weniger A. cerana (47,8 ± 5,9) als A.
melli-fera Arbeiterinnen (51,9 ± 4,6) verrtreten (Tab.I). Die Arbeiterinnen beider Arten zeigten ein völlig normales Hofstaatverhalten gegenüber den hetero-spezifischen Königinnen und wir fanden keine of-fensichtliche Aggression oder ein Vermeidungsver-halten, obwohl sich die Königinnenpheromone der beiden Arten in einigen Punkten unterscheiden. Als Erklärung für die proportionalen Unterschie-de in Unterschie-der Teilnahme am Hofstaatverhalten nehmen wir leichte Abweichungen in den Pheromonen der beiden Arten an. Wir untersuchten deshalb die re-lative Anteile der Komponenten des Königinnen-pheromons in den beiden Typen der Mischvölker (Tab. II). Die Ergebnisse der Multivarianzanalyse
der proportionalen Anteile der Mandibeldrüsen-komponenten zeigten einen signifikanten Unter-schied zwischen A. mellifera und A. cerana (Wilk’s lambda: F= 741, 6, df = 4, 1, P = 0, 027, Tab.II). Während für zwei Komponenten, HOB und 10-HDAA, kein Unterschied zu sehen war, waren die-se für 9-ODA, 9-HDA und 10-HDA signifikant (9-ODA: t= 6, 5, df = 4, P = 0, 003; 9-HDA: t = 7, 4, df = 4, P = 0, 002; 10-HDA: t = 3, 5, df = 4,
P = 0, 024). Der Quotient der
Pheromonkompo-nenten zueinander [9-ODA /(9-ODA+10-HDA+10-HDAA)] war signifikant höher für A. cerana als für A. mellifera Königinnen (t = 3, 0, df = 4,
P= 0, 041, Tab.II). Für beide Arten waren die Kö-niginnen jedoch attraktiv, die Arbeiterinnen bilde-ten eine Hofstaat, beleckbilde-ten die Königin und zeig-ten normales Putz- und Fütterungsverhalzeig-ten. Diese Ergebnisse weisen darauf hin, dass die Hof-staatbildung nicht auf ein spezifisches Königinnen-pheromon oder die Volkssituation zurückzuführen ist, und diese Interpretation stimmt mit bereits pu-blizierten Ergebnissen überein (Pankiw et al.,1994; Hoover et al.,2005). Das nicht artspezifische Hof-staatverhalten in gemischten Kolonien deutet dar-auf hin, dass Königinnenpheromon von Arbeiterin-nen über die Artgrenzen hinweg ohne Hindernisse und unabhängig von möglichen “suppressiven Fak-toren” (Fletcher and Ross,1985) oder “ehrlichen Si-gnalen” (Peeters et al.,1999; Strauss et al.,2008) weitergegeben werden kann. Wir schliessen daraus dass das Hofstaatverhalten selbst, ebenso wie die Könginnenpheromone, die dieses Verhalten indu-zieren, anzestrale, konservierte Merkmale sind, die vor der Artenaufspaltung der apinen Bienen ent-standen sind.
Apis cerana/ Apis mellifera / Hofstaatverhalten /
Königinnenpheromone
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